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Nucleosome eviction and activated transcription require p300 acetylation of histone H3 lysine 14.

Histone posttranslational modifications and chromatin dynamics are inextricably linked to eukaryotic gene expression. Among the many modifications that have been characterized, histone tail acetylation is most strongly correlated with transcriptional activation. In Metazoa, promoters of transcriptio... Full description

Journal Title: Proceedings of the National Academy of Sciences of the United States of America November 9, 2010, Vol.107(45), pp.19254-19259
Main Author: Luebben, Whitney R
Other Authors: Sharma, Neelam , Nyborg, Jennifer K
Format: Electronic Article Electronic Article
Language: English
Subjects:
ID: E-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1009650107
Link: http://search.proquest.com/docview/763471152/?pq-origsite=primo
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recordid: proquest763471152
title: Nucleosome eviction and activated transcription require p300 acetylation of histone H3 lysine 14.
format: Article
creator:
  • Luebben, Whitney R
  • Sharma, Neelam
  • Nyborg, Jennifer K
subjects:
  • Acetyl Coenzyme A–Genetics
  • Acetylation–Metabolism
  • Animals–Metabolism
  • Gene Expression Regulation–Metabolism
  • Histones–Metabolism
  • Lysine–Metabolism
  • Mutation–Metabolism
  • Nucleosomes–Metabolism
  • Promoter Regions, Genetic–Metabolism
  • Transcriptional Activation–Metabolism
  • Histones
  • Nucleosomes
  • Acetyl Coenzyme A
  • Lysine
ispartof: Proceedings of the National Academy of Sciences of the United States of America, November 9, 2010, Vol.107(45), pp.19254-19259
description: Histone posttranslational modifications and chromatin dynamics are inextricably linked to eukaryotic gene expression. Among the many modifications that have been characterized, histone tail acetylation is most strongly correlated with transcriptional activation. In Metazoa, promoters of transcriptionally active genes are generally devoid of physically repressive nucleosomes, consistent with the contemporaneous binding of the large RNA polymerase II transcription machinery. The histone acetyltransferase p300 is also detected at active gene promoters, flanked by regions of histone hyperacetylation. Although the correlation between histone tail acetylation and gene activation is firmly established, the mechanisms by which acetylation facilitates this fundamental biological process remain poorly understood. To explore the role of acetylation in nucleosome dynamics, we utilized an immobilized template carrying a natural promoter reconstituted with various combinations of wild-type and mutant histones. We find that the histone H3 N-terminal tail is indispensable for activator, p300, and acetyl-CoA-dependent nucleosome eviction mediated by the histone chaperone Nap1. Significantly, we identify H3 lysine 14 as the essential p300 acetylation substrate required for dissociation of the histone octamer from the promoter DNA. Together, a total of 11 unique mutant octamer sets corroborated these observations and revealed a striking correlation between nucleosome eviction and strong activator and acetyl-CoA-dependent transcriptional activation. These novel findings uncover an exclusive role for H3 lysine 14 acetylation in facilitating the ATP-independent and transcription-independent disassembly of promoter nucleosomes by Nap1. Furthermore, these studies directly couple nucleosome disassembly with strong, activator-dependent transcription. Tax | chromatin remodeling | cyclic AMP response element binding protein (CREB) | NFR (nucleosome-free region) | HTLV-1 (human T-cell leukemia virus, type 1) doi/ 10.1073/pnas.1009650107
language: eng
source:
identifier: E-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1009650107
fulltext: fulltext
issn:
  • 10916490
  • 1091-6490
url: Link


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titleNucleosome eviction and activated transcription require p300 acetylation of histone H3 lysine 14.
creatorLuebben, Whitney R ; Sharma, Neelam ; Nyborg, Jennifer K
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ispartofProceedings of the National Academy of Sciences of the United States of America, November 9, 2010, Vol.107(45), pp.19254-19259
identifierE-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1009650107
subjectAcetyl Coenzyme A–Genetics ; Acetylation–Metabolism ; Animals–Metabolism ; Gene Expression Regulation–Metabolism ; Histones–Metabolism ; Lysine–Metabolism ; Mutation–Metabolism ; Nucleosomes–Metabolism ; Promoter Regions, Genetic–Metabolism ; Transcriptional Activation–Metabolism ; Histones ; Nucleosomes ; Acetyl Coenzyme A ; Lysine
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descriptionHistone posttranslational modifications and chromatin dynamics are inextricably linked to eukaryotic gene expression. Among the many modifications that have been characterized, histone tail acetylation is most strongly correlated with transcriptional activation. In Metazoa, promoters of transcriptionally active genes are generally devoid of physically repressive nucleosomes, consistent with the contemporaneous binding of the large RNA polymerase II transcription machinery. The histone acetyltransferase p300 is also detected at active gene promoters, flanked by regions of histone hyperacetylation. Although the correlation between histone tail acetylation and gene activation is firmly established, the mechanisms by which acetylation facilitates this fundamental biological process remain poorly understood. To explore the role of acetylation in nucleosome dynamics, we utilized an immobilized template carrying a natural promoter reconstituted with various combinations of wild-type and mutant histones. We find that the histone H3 N-terminal tail is indispensable for activator, p300, and acetyl-CoA-dependent nucleosome eviction mediated by the histone chaperone Nap1. Significantly, we identify H3 lysine 14 as the essential p300 acetylation substrate required for dissociation of the histone octamer from the promoter DNA. Together, a total of 11 unique mutant octamer sets corroborated these observations and revealed a striking correlation between nucleosome eviction and strong activator and acetyl-CoA-dependent transcriptional activation. These novel findings uncover an exclusive role for H3 lysine 14 acetylation in facilitating the ATP-independent and transcription-independent disassembly of promoter nucleosomes by Nap1. Furthermore, these studies directly couple nucleosome disassembly with strong, activator-dependent transcription. Tax | chromatin remodeling | cyclic AMP response element binding protein (CREB) | NFR (nucleosome-free region) | HTLV-1 (human T-cell leukemia virus, type 1) doi/ 10.1073/pnas.1009650107
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